Genetic background and embryonic temperature affect DNA methylation and expression of myogenin and muscle development in Atlantic salmon (Salmo salar)

Abstract

The development of ectothermic embryos is strongly affected by incubation temperature, and thermal imprinting of body growth and muscle phenotype has been reported in various teleost fishes. The complex epigenetic regulation of muscle development in vertebrates involves DNA methylation of the myogenin promoter. Body growth is a heritable and highly variable trait among fish populations that allows for local adaptations, but also for selective breeding. Here we studied the epigenetic effects of embryonic temperature and genetic background on body growth, muscle cellularity and myogenin expression in farmed Atlantic salmon (Salmo salar). Eggs from salmon families with either high or low estimated breeding values for body growth, referred to as Fast and Slow genotypes, were incubated at 8°C or 4°C until the embryonic ‘eyed-stage’ followed by rearing at the production temperature of 8°C. Rearing temperature strongly affected the growth rates, and the 8°C fish were about twice as heavy as the 4°C fish in the order Fast8>Slow8>Fast4>Slow4 prior to seawater transfer. Fast8 was the largest fish also at harvest despite strong growth compensation in the low temperature groups. Larval myogenin expression was approximately 4–6 fold higher in the Fast8 group than in the other groups and was associated with relative low DNA methylation levels, but was positively correlated with the expression levels of the DNA methyltransferase genes dnmt1, dnmt3a and dnmt3b. Juvenile Fast8 fish displayed thicker white muscle fibres than Fast4 fish, while Slow 8 and Slow 4 showed no difference in muscle cellularity. The impact of genetic background on the thermal imprinting of body growth and muscle development in Atlantic salmon suggests that epigenetic variation might play a significant role in the local adaptation to fluctuating temperatures over short evolutionary time.

Marine Environmental Epigenetics

“…Epigenetic alterations were also monitored in marine invertebrates (i.e., bivalve molluscs) exposed to toxins produced by harmful algal blooms, revealing decreased levels of DNA methylation and phosphorylation of histone H2A.X (González-Romero et al 2017). Additional studies have linked DNA methylation and thermal stress in other invertebrates, such as polychaetes (Marsh & Pasqualone 2014), as well as in teleost fishes (Anastasiadi et al 2017, Burgerhout et al 2017.…”

Epigenetic considerations in aquaculture

“…In sea bass and half-smooth tongue sole, temperature-induced sex-determination has been associated with changes in DNA methylation ( Navarro-Martín et al, 2011 ; Shao et al, 2014 ). In salmonids, there is some evidence that changes in DNA methylation are associated with variation in life-history phenotypes including early male maturation ( Morán & Pérez-Figueroa, 2011 ), smoltification ( Morán et al, 2013 ), anadromy ( Baerwald et al, 2016 ) and growth potential ( Burgerhout et al, 2017 ). Recent studies in European sea bass and rainbow trout examined the role of epigenetics in mediating phenotypic responses to various aspects of diet ( Marandel et al, 2016 ; Terova et al, 2016 ; Panserat et al, 2017 ).…”

Influence of feed ration size on somatic and muscle growth in landlocked dwarf and farmed Atlantic salmon Salmo salar

“…The processes underlie adaption to the landlocked habit (Hauge et al, 2016). In support of this idea, we recently reported that effects of genetic background and embryonic temperature on muscle development in S. salar were associated with altered DNA methylation and gene expression of the myogenic regulatory factor myogenin (Burgerhout et al, 2017).…”

“…Relative low genetic variation was shown in the landlocked Namsblank S. salar population (Sandlund et al, ), but genome sequences from a single dwarf fish revealed no loss of coding regions suggesting that fine‐scale (epi)genetic alterations and population genetic processes underlie adaption to the landlocked habit (Hauge et al, ). In support of this idea, we recently reported that effects of genetic background and embryonic temperature on muscle development in S. salar were associated with altered DNA methylation and gene expression of the myogenic regulatory factor myogenin (Burgerhout et al, ).…”